Broad Phylogenetic Diversity Associated with Nitrogen Loss through Sulfur Oxidation in a Large Public Marine Aquarium

• Published in: Applied and environmental microbiology 2018-10, Vol.84 (20)
• Main Authors: Burns, Andrew S, Padilla, Cory C, Pratte, Zoe A, Gilde, Kailen, Regensburger, Matthew, Hall, Eric, Dove, Alistair D M, Stewart, Frank J
• Format: Article
• Language: English
• Subjects: Aquariums; Aquatic environment; Bacteria; Biodiversity; Bioreactors; Chemical analysis; Community involvement; Community structure; Denitrification; Genes; Genomes; Marine technology; Metabolism; Microbial activity; Microbial Ecology; Microorganisms; Nitrate removal; Nitrates; Nitrogen; Nitrogen removal; Nutrient removal; Organic chemistry; Oxidation; Oxidizing agents; Phylogenetics; Phylogeny; Reactors; Retention; Retention time; rRNA 16S; Seawater; Sulfur; Sulfur oxidation; System effectiveness; Taxa; Thiobacillus thioparus; Transcription; Water analysis; Water pollution treatment
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/AEM.01250-18

Denitrification by sulfur-oxidizing bacteria is an effective nitrate removal strategy in engineered aquatic systems. However, the community taxonomic and metabolic diversity of sulfur-driven denitrification (SDN) systems, as well as the relationship between nitrate removal and SDN community structure, remains underexplored. This is particularly true for SDN reactors applied to marine aquaria, despite the increasing use of this technology to supplement filtration. We applied 16S rRNA gene, metagenomic, and metatranscriptomic analyses to explore the microbial basis of SDN reactors operating on Georgia Aquarium's Ocean Voyager, the largest indoor closed-system seawater exhibit in the United States. The exhibit's two SDN systems vary in water retention time and nitrate removal efficiency. The systems also support significantly different microbial communities. These communities contain canonical SDN bacteria, including a strain related to that dominates the system with the higher water retention time and nitrate removal but is effectively absent from the other system. Both systems contain a wide diversity of other microbes whose metagenome-assembled genomes contain genes of SDN metabolism. These include hundreds of strains of the epsilonproteobacterium , as well as gammaproteobacterial sulfur oxidizers of the and , and a relative of with complete denitrification potential. The SDN genes are transcribed and the taxonomic richness of the transcript pool varies markedly among the enzymatic steps, with some steps dominated by transcripts from noncanonical SDN taxa. These results indicate complex and variable SDN communities that may involve chemical dependencies among taxa as well as the potential for altering community structure to optimize nitrate removal. Engineered aquatic systems such as aquaria and aquaculture facilities have large societal value. Ensuring the health of animals in these systems requires understanding how microorganisms contribute to chemical cycling and waste removal. Focusing on the largest seawater aquarium in the United States, we explore the microbial communities in specialized reactors designed to remove excess nitrogen through the metabolic activity of sulfur-consuming microbes. We show that the diversity of microbes in these reactors is both high and highly variable, with distinct community types associated with significant differences in nitrogen removal rate. We also show that the genes encoding the metabolic steps of nitrogen remova